Polygenic adaptation contributes to the invasive success of the Colorado potato beetle

Abstract

Invasive species often experience extreme demographic reductions.A common but counterintuitive phenomenon, the so-called "genetic paradox" of invasion, is that many species still successfully adapt to novel conditions despite heavy reductions in standing genetic variation and effective population size (Allendorf & Lundquist, 2003).Numerous empirical standpoints have emerged to explain this paradox, such as genetic admixture from intra- (Errbii et al., 2021;Kolbe et al., 2004) or interspecies populations (Petit et al., 2004;Wang et al., 2020), activation of transposable elements (Schrader et al., 2014;Stapley et al., 2015), and balancing selection which tends to preserve heterozygosity and prevent the loss of minor alleles (Gloag et al., 2017;Stern & Lee, 2020). However, contingencies and counterexamples prevent coalescence into general rules valid across taxa. Indeed, scepticism has been raised regarding the

Whole genome analyses reveal weak signatures of population structure and environmentally associated local adaptation in an important North American pollinator, the bumble beeBombus vosnesenskii

“…However, a lack of genome regions that show clear associations with temperature is still surprising given recent work on thermal tolerance physiology in B. vosnesenskii (Pimsler et al 2020) that found populations from cold, high elevation habitats had significantly lower critical thermal minima (CT min ) compared to populations from warmer localities (Pimsler et al, 2020). It is possible that selection is weak on individual genes associated with a complex trait like thermal tolerance (Yang, Crossley, Schrader, & Dubovskiy, 2022), that different genes may be targeted by selection in different regions (Yeaman, 2022), or that another non sequence-based mechanism (e.g., epigenetic) could facilitate variation in cold tolerance among populations (Mccaw, Stevenson, & Lancaster, 2020). Detecting selection under the high levels of gene flow that seems prevalent in B. vosnesenskii will also be challenging, and more independent studies, additional sampling, and experimentation will be needed to fully understand any mechanisms of genetic adaptation in this species.…”

Whole genome analyses reveal weak signatures of population structure and environmentally associated local adaptation in an important North American pollinator, the bumble bee Bombus vosnesenskii

“…However, a lack of genome regions that show clear associations with temperature is still surprising given recent work on thermal tolerance physiology in B. vosnesenskii (Pimsler et al, 2020) that found populations from cold, high elevation habitats had significantly lower critical thermal minima (CT min ) compared with populations from warmer localities (Pimsler et al, 2020). It is possible that selection is weak on individual genes associated with a complex trait like thermal tolerance and instead acts on several key genes across a gene regulatory network (Yang et al, 2022). Alternatively, different genes may be targeted by selection in different regions (Yeaman, 2022), or that another nonsequence-based mechanism (e.g.…”

Testing for adaptive changes linked to range expansion following a single introduction of the fall webworm

“…Nevertheless, local adaptation is often considered important in successful invasion (Bock et al, 2015; Lee, 2002; Medley et al, 2019; Szűcs et al, 2017), even though the details of this process are typically unclear (Allendorf & Lundquist, 2003). Many colonized populations have become rapidly structured genetically (Medley et al, 2019; Szucs et al, 2017; Willoughby et al, 2018; Yang et al, 2022), and the relationship between the genetic structure of populations of invasive species and environmental conditions may provide a first step in identifying adaptive changes (Bomblies & Peichel, 2022).…”

“…Several invasive invertebrates have been shown to rapidly evolve and increase population growth after an invasion, such as observed in Drosophila subobscura (Huey et al, 2000), the red‐legged earth mite Halotydeus destructor (Hill et al, 2013), the whitefly Bemisia tabaci (Díaz et al, 2014) and the Colorado potato beetle Leptinotarsa decemlineata (Lehmann et al, 2015). However, most studies on invertebrates have compared the characteristics of native and invasive populations of successful invasive species, whereas fewer studies have considered genetic changes across the invaded range (Comeault et al, 2020; Medley et al, 2019; Yang et al, 2022). Comprehensive sampling across an invaded range, coupled with an assessment of genetic markers across a genome, and fine‐scale analysis of environmental variation should lead to a better understanding of genetic changes that might be associated with adaptation across an invaded range and provide a prelude to further functional and experimental studies.…”